Suppression of mitochondrial biogenesis through toll-like receptor 4-dependent mitogen-activated protein kinase kinase/extracellular signal-regulated kinase signaling in endotoxin-induced acute kidney injury

Journal of Pharmacology and Experimental Therapeutics

Volumn 352, Issue 2, 2015, Pages 346-357

  Smith, Joshua A ^a   Stallons, L Jay ^a   Collier, Justin B ^a   Chavin, Kenneth D ^b   Schnellmann, Rick G ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; KIDNEY INJURY MOLECULE 1; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MULTIENZYME COMPLEX; NEUTRALIZING ANTIBODY; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PLACEBO; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; RTK 2071; TOLL LIKE RECEPTOR 4; TRAMETINIB; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG; ENDOTOXIN; ENDOTOXIN, ESCHERICHIA COLI; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PPARGC1A PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DETERMINATION; DOWN REGULATION; DRUG TARGETING; ENZYME INHIBITION; HOMEOSTASIS; IMMUNOBLOTTING; KIDNEY CORTEX; KIDNEY FUNCTION; KNOCKOUT GENE; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHARMACOLOGICAL BLOCKING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TOXIN ANALYSIS; UREA NITROGEN BLOOD LEVEL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KIDNEY FUNCTION TEST; KNOCKOUT MOUSE; METABOLISM;

ACUTE KIDNEY INJURY; ANIMALS; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTOXINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; KIDNEY CORTEX; KIDNEY FUNCTION TESTS; MALE; MAP KINASE SIGNALING SYSTEM; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTORS;

EID: 84921311514     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.221085     Document Type: Article

References (59)

1. Alvarez-Guardia D, Palomer X, Coll T, Davidson MM, Chan TO, Feldman AM, Laguna JC, and Vázquez-Carrera M (2010) The p65 subunit of NF-κB binds to PGC-1α, linking inflammation and metabolic disturbances in cardiac cells. Cardiovasc Res 87:449-458.
2. Ashabi G, Ramin M, Azizi P, Taslimi Z, Alamdary SZ, Haghparast A, Ansari N, Motamedi F, and Khodagholi F (2012) ERK and p38 inhibitors attenuate memory deficits and increase CREB phosphorylation and PGC-1α levels in Ab-injected rats. Behav Brain Res 232:165-173.
3. Bagshaw SM, Uchino S, Bellomo R, Morimatsu H, Morgera S, Schetz M, Tan I, Bouman C, Macedo E, Gibney N, et al.; Beginning and Ending Supportive Therapy for the Kidney (BEST Kidney) Investigators (2007) Septic acute kidney injury in critically ill patients: clinical characteristics and outcomes. Clin J Am Soc Nephrol 2:431-439.
4. Banerjee A, Gugasyan R, McMahon M, and Gerondakis S (2006) Diverse Toll-like receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc Natl Acad Sci USA 103:3274-3279.
5. Bhargava R, Altmann CJ, Andres-Hernando A, Webb RG, Okamura K, Yang Y, Falk S, Schmidt EP, and Faubel S (2013) Acute lung injury and acute kidney injury are established by four hours in experimental sepsis and are improved with pre, but not post, sepsis administration of TNF-α antibodies. PLoS ONE 8:e79037.
6. Chawla LS, Seneff MG, Nelson DR, Williams M, Levy H, Kimmel PL, and Macias WL (2007) Elevated plasma concentrations of IL-6 and elevated APACHE II score predict acute kidney injury in patients with severe sepsis. Clin J Am Soc Nephrol 2:22-30.
7. Che R, Yuan Y, Huang S, and Zhang A (2014) Mitochondrial dysfunction in the pathophysiology of renal diseases. Am J Physiol Renal Physiol 306:F367-F378.
8. Coll T, Jové M, Rodríguez-Calvo R, Eyre E, Palomer X, Sánchez RM, Merlos M, Laguna JC, and Vázquez-Carrera M (2006) Palmitate-mediated downregulation of peroxisome proliferator-activated receptor-gamma coactivator 1a in skeletal muscle cells involves MEK1/2 and nuclear factor-κB activation. Diabetes 55: 2779-2787.
9. Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, and Quigg RJ (2002) Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168:5817-5823.
10. Cunningham PN, Wang Y, Guo R, He G, and Quigg RJ (2004) Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 172:2629-2635.
11. DeFranco AL, Crowley MT, Finn A, Hambleton J, and Weinstein SL (1998) The role of tyrosine kinases and map kinases in LPS-induced signaling. Prog Clin Biol Res 397:119-136.
12. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, Lin JH, Patriotis C, Jenkins NA, Copeland NG, Kollias G, et al. (2000) TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103: 1071-1083.
13. Ellett JD, Evans ZP, Atkinson C, Schmidt MG, Schnellmann RG, and Chavin KD (2009) Toll-like receptor 4 is a key mediator of murine steatotic liver warm ischemia/reperfusion injury. Liver Transplant 15:1101-1109.
14. Finck BN and Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116:615-622.
15. Funk JA and Schnellmann RG (2012) Persistent disruption of mitochondrial homeostasis after acute kidney injury. Am J Physiol Renal Physiol 302:F853-F864.
16. Funk JA and Schnellmann RG (2013) Accelerated recovery of renal mitochondrial and tubule homeostasis with SIRT1/PGC-1α activation following ischemiareperfusion injury. Toxicol Appl Pharmacol 273:345-354.
17. Gilmartin AG, Bleam MR, Groy A, Moss KG, Minthorn EA, Kulkarni SG, Rominger CM, Erskine S, Fisher KE, Yang J, et al. (2011) GSK1120212 (JTP-74057) is an inhibitor of MEK activity and activation with favorable pharmacokinetic properties for sustained in vivo pathway inhibition [erratum: 2012;15:2413]. Clin Cancer Res 17: 989-1000.
18. Gomez H, Ince C, De Backer D, Pickkers P, Payen D, Hotchkiss J, and Kellum JA (2014) A unified theory of sepsis-induced acute kidney injury: inflammation, microcirculatory dysfunction, bioenergetics, and the tubular cell adaptation to injury. Shock 41:3-11.
19. Gottlieb RA and Gustafsson AB (2011) Mitochondrial turnover in the heart. Biochim Biophys Acta 1813:1295-1301.
20. Guha M, O'Connell MA, Pawlinski R, Hollis A, McGovern P, Yan SF, Stern D, and Mackman N (2001) Lipopolysaccharide activation of the MEK-ERK1/2 pathway in human monocytic cells mediates tissue factor and tumor necrosis factor alpha expression by inducing Elk-1 phosphorylation and Egr-1 expression. Blood 98:1429-1439.
21. Guo R, Wang Y, Minto AW, Quigg RJ, and Cunningham PN (2004) Acute renal failure in endotoxemia is dependent on caspase activation. J Am Soc Nephrol 15: 3093-3102.
22. Hagar JA, Powell DA, Aachoui Y, Ernst RK, and Miao EA (2013) Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341:1250-1253.
23. Jesinkey SR, Funk JA, Stallons LJ, Wills LP, Megyesi JK, Beeson CC, and Schnellmann RG (2014) Formoterol restores mitochondrial and renal function after ischemiareperfusion injury. J Am Soc Nephrol 25:1157-1162.
24. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszyński A, et al. (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341: 1246-1249.
25. Knotek M, Rogachev B, Wang W, Ecder T, Melnikov V, Gengaro PE, Esson M, Edelstein CL, Dinarello CA, and Schrier RW (2001) Endotoxemic renal failure in mice: role of tumor necrosis factor independent of inducible nitric oxide synthase. Kidney Int 59:2243-2249.
26. Langenberg C, Bagshaw SM, May CN, and Bellomo R (2008) The histopathology of septic acute kidney injury: a systematic review. Crit Care 12:R38.
27. Lin M and Tang SC (2014) Toll-like receptors: sensing and reacting to diabetic injury in the kidney. Nephrol Dial Transplant 29:746-754.
28. Luan H, Zhang Q, Wang L, Wang C, Zhang M, Xu X, Zhou H, Li X, Xu Q, He F, Yuan J, and Lv Y (2014) OM85-BV induced the productions of IL-1b, IL-6, and TNF-α via TLR4-and TLR2-mediated ERK1/2/NF-κB pathway in RAW264.7 cells. J Interferon Cytokine Res 34:526-536.
29. Nowak G, Aleo MD, Morgan JA, and Schnellmann RG (1998) Recovery of cellular functions following oxidant injury. Am J Physiol 274:F509-F515.
30. Ostuni R, Zanoni I, and Granucci F (2010) Deciphering the complexity of Toll-like receptor signaling. Cell Mol Life Sci 67:4109-4134.
31. Patil NK, Parajuli N, MacMillan-Crow LA, and Mayeux PR (2014) Inactivation of renal mitochondrial respiratory complexes and manganese superoxide dismutase during sepsis: mitochondria-targeted antioxidant mitigates injury. Am J Physiol Renal Physiol 306:F734-F743.
32. Portilla D, Dai G, McClure T, Bates L, Kurten R, Megyesi J, Price P, and Li S (2002) Alterations of PPARa and its coactivator PGC-1 in cisplatin-induced acute renal failure. Kidney Int 62:1208-1218.
33. Puigserver P, Wu Z, Park CW, Graves R, Wright M, and Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839.
34. Remels AH, Gosker HR, Bakker J, Guttridge DC, Schols AM, and Langen RC (2013) Regulation of skeletal muscle oxidative phenotype by classical NF-κB signalling. Biochim Biophys Acta 1832:1313-1325.
35. Sanchis-Gomar F, García-Giménez JL, Gómez-Cabrera MC, and Pallardó FV (2014) Mitochondrial biogenesis in health and disease. Molecular and therapeutic approaches. Curr Pharm Des 20:5619-5633.
36. Scarpulla RC (2011) Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta 1813:1269-1278.
37. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Götte M, et al. (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115:2223-2233.
38. Schrier RW and Wang W (2004) Acute renal failure and sepsis. N Engl J Med 351: 159-169.
39. Silvester W, Bellomo R, and Cole L (2001) Epidemiology, management, and outcome of severe acute renal failure of critical illness in Australia. Crit Care Med 29: 1910-1915.
40. Soltoff SP (1986) ATP and the regulation of renal cell function. Annu Rev Physiol 48: 9-31.
41. Stallons LJ, Funk JA, and Schnellmann RG (2013) Mitochondrial homeostasis in acute organ failure. Curr Pathobiol Rep 1:169-177.
42. Stallons LJ, Whitaker RM, and Schnellmann RG (2014) Suppressed mitochondrial biogenesis in folic acid-induced acute kidney injury and early fibrosis. Toxicol Lett 224:326-332.
43. Sweeney TE, Suliman HB, Hollingsworth JW, and Piantadosi CA (2010) Differential regulation of the PGC family of genes in a mouse model of Staphylococcus aureus sepsis. PLoS ONE 5:e11606.
44. Takasu O, Gaut JP, Watanabe E, To K, Fagley RE, Sato B, Jarman S, Efimov IR, Janks DL, Srivastava A, et al. (2013) Mechanisms of cardiac and renal dysfunction in patients dying of sepsis. Am J Respir Crit Care Med 187:509-517.
45. Thadhani R, Pascual M, and Bonventre JV (1996) Acute renal failure. N Engl J Med 334:1448-1460.
46. Tran M, Tam D, Bardia A, Bhasin M, Rowe GC, Kher A, Zsengeller ZK, Akhavan-Sharif MR, Khankin EV, Saintgeniez M, et al. (2011) PGC-1α promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest 121: 4003-4014.
47. Uchino S, Kellum JA, Bellomo R, Doig GS, Morimatsu H, Morgera S, Schetz M, Tan I, Bouman C, Macedo E, et al.; Beginning and Ending Supportive Therapy for the Kidney (BEST Kidney) Investigators (2005) Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA 294:813-818.
48. Waikar SS, Liu KD, and Chertow GM (2008) Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol 3:844-861.
49. Wan L, Bagshaw SM, Langenberg C, Saotome T, May C, and Bellomo R (2008) Pathophysiology of septic acute kidney injury: what do we really know? Crit Care Med 36(4, Suppl)S198-S203.
50. Wang Z, Herzog C, Kaushal GP, Gokden N, and Mayeux PR (2011) Actinonin, a meprin A inhibitor, protects the renal microcirculation during sepsis. Shock 35: 141-147.
51. Watts BA, 3rd, George T, and Good DW (2013) Lumen LPS inhibits HCO3-absorption in the medullary thick ascending limb through TLR4-PI3K-Akt-mTORdependent inhibition of basolateral Na1/H1 exchange. Am J Physiol Renal Physiol 305:F451-F462.
52. Weinberg JM (2011) Mitochondrial biogenesis in kidney disease. J Am Soc Nephrol 22:431-436.
53. Wills LP, Trager RE, Beeson GC, Lindsey CC, Peterson YK, Beeson CC, and Schnellmann RG (2012) The β2-adrenoceptor agonist formoterol stimulates mitochondrial biogenesis. J Pharmacol Exp Ther 342:106-118.
54. Wu L, Gokden N, and Mayeux PR (2007a) Evidence for the role of reactive nitrogen species in polymicrobial sepsis-induced renal peritubular capillary dysfunction and tubular injury. J Am Soc Nephrol 18:1807-1815.
55. Wu L, Tiwari MM, Messer KJ, Holthoff JH, Gokden N, Brock RW, and Mayeux PR (2007b) Peritubular capillary dysfunction and renal tubular epithelial cell stress following lipopolysaccharide administration in mice. Am J Physiol Renal Physiol 292:F261-F268.
56. Xu C, Chang A, Hack BK, Eadon MT, Alper SL, and Cunningham PN (2014) TNFmediated damage to glomerular endothelium is an important determinant of acute kidney injury in sepsis. Kidney Int 85:72-81.
57. Yamaguchi T, Kakefuda R, Tajima N, Sowa Y, and Sakai T (2011) Antitumor activities of JTP-74057 (GSK1120212), a novel MEK1/2 inhibitor, on colorectal cancer cell lines in vitro and in vivo. Int J Oncol 39:23-31.
58. Yamaguchi T, Kakefuda R, Tanimoto A, Watanabe Y, and Tajima N (2012) Suppressive effect of an orally active MEK1/2 inhibitor in two different animal models for rheumatoid arthritis: a comparison with leflunomide. Inflamm Res 61:445-454.
59. Yaomura T, Tsuboi N, Urahama Y, Hobo A, Sugimoto K, Miyoshi J, Matsuguchi T, Reiji K, Matsuo S, and Yuzawa Y (2008) Serine/threonine kinase, Cot/Tpl2, regulates renal cell apoptosis in ischaemia/reperfusion injury. Nephrology (Carlton) 13: 397-404.